High frequency of delayed milk delivery to neonates in tropical beef herds

Abstract Beef‐calf mortality rates across tropical and subtropical Australia are high, with sub‐optimal nutrition in pregnant cows being the primary risk. The nutritional deficiencies associated with calf mortality are the same as those associated with reduced milk yields. Although the highest mortality risk occurs during neonatal life, the role of inadequate milk delivery to beef neonates is not well established. This study investigated the frequency of low milk delivery in tropically adapted neonatal calves and the time for their dams to initiate full lactation in five management groups of Brahman and Droughtmaster calving cows in the dry tropics of northern Queensland, Australia. Change in calf weight in the days following birth was the primary measure of milk uptake. Plasma globulin concentration was used to indicate colostrum uptake. Across management groups, data were available on 250 calves for regression analysis of average daily gain vs. globulin and on 78 for plotting calf growth profiles. Calves had one of two growth profiles, either with immediate high growth from birth (day one) or with high growth delayed until day three. The frequency of delayed growth calves (with inadequate milk intake to gain at least 0.5 kg by day three after birth) was on average 30% across management groups, with management groups ranging 25%–50%. The frequency of calves growing ≤0.2 kg/day to day three was 15%–37%, depending on management group. The frequency of calves growing ≤0.2 kg/day to day five was 7%–20%, depending on management group. Calf globulin explained only 25% of the variation in calf average daily gain. Our study shows that a third of tropically adapted calves may experience a three‐day delay to initiation of full lactation by their dams. Although study conditions were relatively benign, any additional risks with milk delivery, such as those that occur widely in tropical and subtropical northern Australia, would place such calves at risk of dehydration and mortality. Calf plasma globulin should not be used as a standalone measure of adequacy of neonatal milk delivery, especially when comparing across herds. This study demonstrates a fundamental problem of high frequency in northern Australia. The underlying risks for delayed milk delivery should be considered in the quest for practical solutions to reduce tropically adapted beef‐calf mortalities.


| INTRODUC TI ON
Calf wastage (reproductive loss between confirmed pregnancy and weaning) has significant impacts on production (Fordyce et al., 2021) and animal welfare (Mee et al., 2019;Mellor & Stafford, 2004). Calf wastage levels in tropical and subtropical Australian beef herds are typically 5%-15%, where levels exceeding 20% are not uncommon, and can be up to 40% (McCosker et al., 2020). Calf wastage is also prevalent in other tropical countries, with levels averaging 8%-48% for various regions of Indonesia (Talib et al., 2003) and 11%-23% for various regions of West Timor (Jelantik et al., 2008). The highest risk period for calf wastage is during neonatal life (the first week from birth), in both temperate herds (Bendali et al., 1999;Mõtus et al., 2018) and in tropical herds, where neonatal mortality accounts for two-thirds of calf wastage (Bunter et al., 2013). Before the specific mechanisms explaining neonatal mortality may be investigated in tropical beef calves, the risk factors for overall calf wastage in commercial herds must be considered. Herds exposed to poor pre-partum nutrition consistently have increased calf wastage . In addition, high ambient heat load around calving is associated with increased calf wastage within three of the four major land types in tropical and subtropical Australia . Both poor pre-partum nutrition for cows and high ambient heat loads around calving are risks that occur frequently across tropical and subtropical Australian herds. A decline in pasture digestibility and protein content occurs during the dry season in northern Australia (McIvor, 1981;Norman, 1963;Robinson & Sageman, 1967;Squires & Siebert, 1983), which typically occurs from March through to November-January. Peak calving in northern Australia occurs around the end of dry season (Bortolussi et al., 2005), that is late spring-summer. Therefore, the progression of pregnancy in cows coincides with a decrease in the quality of diet selected from the pasture, and calving cows are exposed to increasing ambient heat loads. The reason for timing reproduction in this way is to optimize overall reproductive performance and production (Hamlyn-Hill, 2011;McCosker et al., 2022).
While the primary risk factors for overall calf wastage provide useful context , the majority of neonatal mortalities in tropical beef herds remain unexplained (Bunter et al., 2013). The nutritional deficiencies associated with calf wastage are the same as those associated with reduced milk yields, especially deficiencies of energy (Banchero et al., 2015), protein (Cowan et al., 1980), phosphorus (Castells et al., 2014) and water (Murphy et al., 1983). While high ambient heat loads around calving are associated with increased calf wastage , they are also associated with reduced milk yields (Brody, 1956;West et al., 2003). If neonatal calves do not receive milk, they die within three days at comfortable ambient temperature or within one day under hot conditions (Fordyce et al., 2015). The key mechanism mediating the effects of nutritional deficiency and/or high heat loads on calf mortality in tropical and subtropical Australia may therefore be low milk delivery and dehydration within the first week of birth.
A lack of colostrum delivery, and thus, failure of passive immunity transfer is a major contributor to calf morbidity and mortality in intensively managed beef and dairy herds (Pérez et al., 1998).
The relationship between level of passive transfer and mortality is well established in dairy calves (e.g. Donovan et al., 1998;Ibrahim & Lemma, 2009;Tyler et al., 1998), and there are some studies on failure of passive transfer to beef neonates in temperate environments (Filteau et al., 2003;Todd et al., 2018). In these production systems, failure of passive transfer predisposes neonates to diseases including diarrhoea and respiratory disease, which consequently are the most common causes of mortality and morbidity in young dairy cattle (Windeyer et al., 2014). The risk factors for calf mortality and morbidity in intensive systems include high stocking rate of calving cows (Radostits & Acres, 1980;Sanderson & Dargatz, 2000), cool moist conditions where all major enteric pathogens can survive for weeks to months (Anon., 2005;Millemann, 2009), contaminated environments (Cho & Yoon, 2014) and poor drainage (Radostits & Acres, 1980;Schumann et al., 1990;Singh et al., 2019). Risk factors are vastly different in tropical, extensively managed production systems, which are characterized by far lower stocking rates on lower quality pasture, and often extreme ambient heat through the calving period. In addition, calves in intensive systems that experience diarrhoea typically experience hyponatraemic dehydration (Groutides et al., 1990), secondary to fluid and solute loss through diarrhoea.
This differs to dehydration in healthy milk-deprived neonates that experience hypernatraemic dehydration, that is progressive loss of fluids while solutes are retained at an increasing concentration (Fordyce et al., 2015).
Colostrum uptake may be assessable using plasma globulin concentration (Zanker et al., 2001) as calves are born practically agammaglobulinaemic (Cabral et al., 2012). Milk delivery to calves may also be quantifiable by their weight change, as accrual of solid and fluid as tissue is primarily a function of milk uptake (Bartle et al., 1982;Black, 1982;Montsma, 1960;Totusek et al., 1973), and milk-deprived calves lose weight primarily through body water loss (Fordyce et al., 2015).
The timing and frequency of low milk delivery in suckling neonatal beef calves in tropical environments have, however, not been investigated. If low milk delivery occurs at significant frequency, there may be opportunities to increase calf survival rates by managing cows so they produce and deliver adequate colostrum and milk for neonates. This study investigated the following in neonatal calves of tropical beef cattle herds: (1) What is the highest risk period for low

| Site calving environments
The study was conducted in the northern forest region of the

| Animal management
Calving occurred mid-dry season for SPY-NP and late-dry season for all other management groups (Table 1).

SPY-NP.
Cows grazed the study paddock in the weeks prior to and during calving and were allowed ad libitum access to a supplement with expected individual daily intake of approximately 120 g (comprising 87% CP, 3.6% Ca, 3.4% P, 2.9% S, 1.5% fibre, 0.04% Mg and 1.96 MJ ME/kg).
SPY-P and FV-P. As part of an experiment, cows grazed in a paddock (one paddock per site) throughout pregnancy until birth of the first calf whereafter all animals were transferred to pens (on 5 October 2018 for SPY-P and 12 November 2018 for FV-P). At SPY-P, cows were stratified based on live weight into two replicates, with each replicate containing three pens of different nutritional treatments: (1) Low-quality Rhodes grass (Chloris gayana) hay fed ad libitum; (2) Rhodes grass hay plus 1.0 kg/cow day of a protein supplement (as fed: DM 91%, 35.5% CP, 7.9 MJ ME/kg); or, (3) The Rhodes grass hay plus the protein supplement with 14 g/cow of an added yeast extract (NaturSafe®, Diamond V). At FV-P, cows were allocated into pens in the same way, but to only one replicate of the TA B L E 1 Description of cattle management groups assessed for variation in milk delivery to neonatal calves

| Measurements
In all management groups, cows were assessed for body condition score (1-5, 1 = emaciated and 5 = obese) on the day their calf was first assessed.
SPY-NP calves and their dams were mustered daily from the day of birth until day seven of neonatal life, by a horseman between approximately 6:30 am and noon to cattle yards adjacent to the paddock. On a daily basis, calves were weighed to the nearest 0.5 kg using an aluminium platform scale (Ruddweigh Gallagher) and ~ 6 ml blood was sampled from the jugular into heparinized vacutainers that were placed immediately in an ice-water bath until centrifugation and plasma collection 1-4 h later. Plasma samples were frozen for subsequent assays.

| Data management and statistical analyses
Separate analyses were conducted to (1)  classes for globulin within management groups SPY-P and FV-P were completed using the same terms, but in anova analyses, given data for only days one and three were available.
To determine whether there was a relationship between calf ADG and globulin, calf ADG was analysed using grouped linear regression, with explanatory variables: calf average globulin, management group and their interaction. The regression assumption of normally distributed residuals was tested by using normal probability plots. For the regression analysis, globulin values of calves were TA B L E 2 Counts of available data for regression analysis, plotting growth profiles, and counts of cows exposed to different supplementation treatments

F I G U R E 1
Growth from birth (± SE) for calves with immediate growth (▲) and delayed growth (■) from birth, using values predicted by restricted maximum likelihood (REML) analyses. Acronyms denote the environment in which calving occurred for each management group: SPY-NP: Native pasture at Spyglass Beef Research Facility, SPY-P: Pens at Spyglass, FV-P: Pens at Fletcherview Research Station. * significant difference between growth profiles on a particular day within a calving environment; # significant growth from birth within a growth profile averaged to provide one datapoint per calf. Across management groups, the total number of calves with data available for both ADG and plasma globulin was 250. Available datapoints per management group and supplementation treatment are reported in Table 2. For SPY-IP2, the early-and late-calving cows were considered as separate management groups in the regression, given there was adequate sample size to do so (n = 40 and 47, respectively). Due to confounding with management group, other variables were not investigated in the regression analysis, including breed, cow age, cow body condition at day of calving, and whether cows were supplemented prior to calving or not (1 or 0).

| RE SULTS
It was found that calves had one of two classes of growth profile, immediate growth from the day of birth (day one) or with growth from birth delayed until day three (Figure 1). The frequency of calves with delayed growth (not achieving at least 0.5 kg by day three) was 29% for SPY-NP, 25% for SPY-P and 50% for FV-P, and was 30.8% across calves in these three management groups. Delayed growth calves and immediate growth calves did not differ in birth weight for SPY-NP (31.1 ± 2.9 vs. 27.9 ± 4.3 kg, p = .15); SPY-P (30.4 ± 2.8 vs. 32.0 ± 3.8, p = .15); and FV-P (30.7 ± 2.8 vs. 30.2 ± 5.3, p = .82). Dams of delayed growth and immediate growth calves did not differ for age at calving for SPY-NP (5.1 ± 0.89 and 4.9 ± 0.9 years respectively, p = .59) and FV-P (5.3 ± 1.9 and 5.9 ± 2.7 years respectively, p = .84). Globulin and day of neonatal life were not associated for SPY-P (p = .13) but were for FV-P (p = .04). The interaction between growth profile and age was not significant for SPY-P and FV-P (p = .32 and .84, respectively).
Though there was no relationship between calf ADG and globulin when management group was not included in the regression model (p = .11), it was significant with management group included (p < .001; Table 3). The interaction between globulin and management group was not significant (p = .95).

| DISCUSS ION
In this study, a third of tropically adapted suckling neonates barely received adequate milk to grow during the first three days of neonatal life. Timely milk delivery during the first three days of neonatal life is critical for calf survival, as milk-deprived tropically adapted calves die within three days, even under comfortable ambient temperatures (Fordyce et al., 2015). Delayed milk-delivery calves are hypothesized to be at higher risk of dehydration and mortality where additional risk factors for low milk delivery exist. Compared with cows in the current study, risk levels for inadequate milk delivery to neonatal calves are expected to be much higher in many commercial herds in northern Australia, particularly where nutrition is limited due to poor quality and/or inadequate forage. Many commercial paddocks are much larger than the study paddocks, with waters far apart, placing additional stress on cows. Although low colostrum intake by calves may explain a significant proportion of the calf mortalities occurring in northern Australia , the link between milk delivery within the first three days of birth, that is the period of colostrum delivery (Crowther et al., 1916), and risk of calf mortality has not been established in tropical beef calves, as it has in dairy calves (Donovan et al., 1998) and piglets (Quesnel et al., 2012).
The risk of delayed growth in calves occurred in both Brahman and Droughtmaster herds, and across different years and sites. The reoccurrence of this risk supports the hypothesis that an underlying fundamental mechanism is driving the delay. The environmental risks and biological mechanisms explaining the differential timing of milk delivery between neonates are unclear. Although the variation in timing and volume of milk delivery to beef neonates is poorly understood, it may be explained by variation in calf ability to stand and suckle (Kim et al., 1988) and/or variation in peri-partum milk yields.
As dams of both immediate-and delayed-milk delivery calves were of the same age, cow age does not explain the difference. In the current study, there was a very low frequency of weak calves (data not shown), precluding investigation of effects of this risk factor on milk delivery. Cows would be at increased risk of delivering weak calves if on a low protein diet pre-partum (Bull et al., 1974) where weak calves have delayed suckling after birth (Kim et al., 1988). While it appears that milk yields may be a primary contributor to the high frequency of inadequate neonatal milk delivery in this study, subclinical effects on calves due to calving difficulty should not be discounted. Delayed milk delivery has been reported in other species, including humans. In women, very limited milk yields have been reported in the first two days post-partum, with rapid increase in production by days three-four post-partum, where milk yields were measured by change in weight of infants (Neville et al., 1988;Saint et al., 1984).
In dairy cows, there is limited secretion of milk components in pregnancy (lactogenesis I). Copious secretion of key milk components including lactose, and consequent osmotic accumulation of milk fluid (lactogenesis II; McCance et al., 1959), does not occur until the fourday pre-partum period in dairy cows (Hartmann, 1973 where weight change has been shown to be an accurate measure of milk uptake in infants (Meier et al., 1990;Scanlon et al., 2002) and has been associated with milk uptake in dairy calves fed known amounts of milk (Huber et al., 1984;Khouri et al., 1968). ADG in young, pre-weaned calves can be influenced by factors other than calf globulin, including cow body condition (McBryde et al., 2013;Winks et al., 1978), breed (Silveira et al., 2019), cow parity (Fordyce et al., 1993;Silveira et al., 2019), and management and environmental factors around the calving period including forage quantity/ quality available (Fordyce et al., 1993), supplementation strategy (Short et al., 1996;Silva et al., 2022) and ambient heat load (Shivley et al., 2018). Though these animals, management and environmental factors can have large effects on overall milk yields, they can also have effects on colostrum globulin concentration (Shearer et al., 1992). Therefore, the effects of these factors on overall calf ADG may be at least partially explained by colostrum globulin concentration. While these factors were not considered in this study, including management group in the regression analysis corrected for some of their variation and increased the strength of association between ADG and globulin. Despite a link between calf circulating globulin concentration and neonatal growth, as has occurred in dairy calves (Elsohaby et al., 2019a), globulin was not an accurate predictor of neonatal ADG across different management groups.
Therefore, a globulin threshold value was not identified, and globulin cannot be used as a stand-alone measure to quantify milk delivery to neonates.
Further research is required to determine the specific risks associated with delayed or low milk delivery to tropically adapted beef neonates, especially that related to cow diet quality selected from pasture, supplementation strategy and ambient heat loads. If the use of neonatal calf live weight change as a measure of milk delivery, with cognisance of both quantity and quality of milk, can be further verified, it will increase the ease of calf survival research. Milk delivery to neonatal calves should be a primary consideration in studies of interventions such as the strategic use of high-quality pastures and/or dam supplements for reducing calf mortality in tropical and subtropical regions.

| CON CLUS ION
Approximately a third of tropically adapted calves may experience a three-day delay to initiation of full lactation by their dams. The risk of delayed milk delivery may place calves at higher risk of mortality under conditions that decrease potential milk production, increase the requirements of neonates for milk and/or reduce the capacity of the neonate to access milk. This risk appears to reduce after day four of neonatal life. Reduced colostrum delivery may also reduce immunocompetence and contribute further to risk of suckling-calf mortality. Calf circulating globulin concentration is related to, though does not accurately predict calf growth and therefore overall milk delivery to neonatal calves. Consequently, a useful globulin threshold was not identified.

AUTH O R CO NTR I B UTI O N S
Jarud Muller contributed to experimental design, project administration, managing and conducting field work, and writing. Luis Silva contributed to experimental design, project administration, supervision of project for management groups SPY-P and FV-P, and writing.
Geoffry Fordyce contributed to experimental design, project administration, funding acquisition, overall supervision of all management groups, and writing.

CO N FLI C T O F I NTE R E S T
None of the authors have any conflict of interest to declare.

DATA AVA I L A B I L I T Y
The data that support the findings of this study are available from the corresponding author upon reasonable request.